Ancient DNA of the pygmy marmoset type specimen <i>Cebuella pygmaea</i> (Spix, 1823) resolves a taxonomic conundrum

Jean P. Boubli; Mareike C. Janiak; Leila M. Porter; Stella de la Torre; Liliana Cortés-Ortiz; Maria N. F. da Silva; Anthony B. Rylands; Stephen Nash; Fabrício Bertuol; Hazel Byrne; Felipe E. Silva; Fabio Rohe; Dorien de Vries; Robin M. D. Beck; Irune Ruiz-Gartzia; Lukas F. K. Kuderna; Tomas Marques-Bonet; Tomas Hrbek; Izeni P. Farias; Anneke H. van Heteren; Christian Roos

doi:10.24272/j.issn.2095-8137.2021.143

Volume 42 Issue 6

Nov. 2021

Turn off MathJax

Article Contents

Article Navigation > Zoological Research > 2021 > 42(6): 761-771

Jean P. Boubli, Mareike C. Janiak, Leila M. Porter, Stella de la Torre, Liliana Cortés-Ortiz, Maria N. F. da Silva, Anthony B. Rylands, Stephen Nash, Fabrício Bertuol, Hazel Byrne, Felipe E. Silva, Fabio Rohe, Dorien de Vries, Robin M. D. Beck, Irune Ruiz-Gartzia, Lukas F. K. Kuderna, Tomas Marques-Bonet, Tomas Hrbek, Izeni P. Farias, Anneke H. van Heteren, Christian Roos. Ancient DNA of the pygmy marmoset type specimen Cebuella pygmaea (Spix, 1823) resolves a taxonomic conundrum. Zoological Research, 2021, 42(6): 761-771. doi: 10.24272/j.issn.2095-8137.2021.143

Citation:

Jean P. Boubli, Mareike C. Janiak, Leila M. Porter, Stella de la Torre, Liliana Cortés-Ortiz, Maria N. F. da Silva, Anthony B. Rylands, Stephen Nash, Fabrício Bertuol, Hazel Byrne, Felipe E. Silva, Fabio Rohe, Dorien de Vries, Robin M. D. Beck, Irune Ruiz-Gartzia, Lukas F. K. Kuderna, Tomas Marques-Bonet, Tomas Hrbek, Izeni P. Farias, Anneke H. van Heteren, Christian Roos. Ancient DNA of the pygmy marmoset type specimen Cebuella pygmaea (Spix, 1823) resolves a taxonomic conundrum. Zoological Research, 2021, 42(6): 761-771. doi: 10.24272/j.issn.2095-8137.2021.143

Citation:

Jean P. Boubli, Mareike C. Janiak, Leila M. Porter, Stella de la Torre, Liliana Cortés-Ortiz, Maria N. F. da Silva, Anthony B. Rylands, Stephen Nash, Fabrício Bertuol, Hazel Byrne, Felipe E. Silva, Fabio Rohe, Dorien de Vries, Robin M. D. Beck, Irune Ruiz-Gartzia, Lukas F. K. Kuderna, Tomas Marques-Bonet, Tomas Hrbek, Izeni P. Farias, Anneke H. van Heteren, Christian Roos. Ancient DNA of the pygmy marmoset type specimen Cebuella pygmaea (Spix, 1823) resolves a taxonomic conundrum. Zoological Research, 2021, 42(6): 761-771. doi: 10.24272/j.issn.2095-8137.2021.143

PDF( 7289 KB)

Ancient DNA of the pygmy marmoset type specimen Cebuella pygmaea (Spix, 1823) resolves a taxonomic conundrum

doi: 10.24272/j.issn.2095-8137.2021.143

1.
School of Science, Engineering & Environment, University of Salford, Salford M5 4WT, UK
2.
Instituto Nacional de Pesquisas da Amazônia, Manaus, Amazonas 69060-001, Brazil
3.
Department of Anthropology, Northern Illinois University, DeKalb, IL 60115-2828, USA
4.
College of Biological and Environmental Sciences, Universidad San Francisco de Quito, Quito 170901, Ecuador
5.
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
6.
Re:wild, Austin, TX 78767, USA
7.
Laboratório de Evolução e Genética Animal, Universidade Federal do Amazonas, Manaus, Amazonas 69080-900, Brazil
8.
Department of Anthropology, University of Utah, Salt Lake City, UT 84112, USA
9.
Research Group on Primate Biology and Conservation, Mamirauá Institute for Sustainable Development, Tefé, Amazonas 69553-225, Brazil
10.
Experimental and Health Sciences Department (DCEXS), Institut de Biologia Evolutiva, Universitat Pompeu Fabra-CSIC, Barcelona 08002, Spain
11.
Department of Biology, Trinity University, San Antonio, TX 78212, USA
12.
Bavarian State Collection of Zoology, Zoologische Staatssammlung München, Staatliche Naturkundliche Sammlungen Bayerns, 81247 Munich, Germany
13.
GeoBio-Center, Ludwig-Maximilians-Universität München, 80333 Munich, Germany
14.
Department Biologie II, Ludwig-Maximilians-Universität München, 82152 Munich, Germany
15.
Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, 37077 Göttingen, Germany

Funds: This study was supported by the Conselho Nacional de Pesquisa, Brazil (563348/2010), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (3261/2013), NSF (1241066), FAPESP (12/50260-6) and NERC (NE/T000341/1)

More Information

Corresponding author: E-mail: j.p.boubli@salford.ac.uk
Received Date: 2021-08-20
Accepted Date: 2021-10-08

Published Online: 2021-10-12

Publish Date: 2021-11-18

Abstract

Abstract

The pygmy marmoset, the smallest of the anthropoid primates, has a broad distribution in Western Amazonia. Recent studies using molecular and morphological data have identified two distinct species separated by the Napo and Solimões-Amazonas rivers. However, reconciling this new biological evidence with current taxonomy, i.e., two subspecies, Cebuella pygmaea pygmaea (Spix, 1823) and Cebuella pygmaea niveiventris (Lönnberg, 1940), was problematic given the uncertainty as to whether Spix’s pygmy marmoset (Cebuella pygmaea pygmaea) was collected north or south of the Napo and Solimões-Amazonas rivers, making it unclear to which of the two newly revealed species the name pygmaea would apply. Here, we present the first molecular data from Spix’s type specimen of Cebuella pygmaea, as well as novel mitochondrial genomes from modern pygmy marmosets sampled near the type locality (Tabatinga) on both sides of the river. With these data, we can confirm the correct names of the two species identified, i.e., C. pygmaea for animals north of the Napo and Solimões-Amazonas rivers and C. niveiventris for animals south of these two rivers. Phylogenetic analyses of the novel genetic data placed into the context of cytochrome b gene sequences from across the range of pygmy marmosets further led us to re-evaluate the geographical distribution for the two Cebuella species. We dated the split of these two species to 2.54 million years ago. We discuss additional, more recent, subdivisions within each lineage, as well as potential contact zones between the two species in the headwaters of these rivers.
- Historic DNA,
- DNA taxonomy,
- Pygmy marmoset,
- Cebuella pygmaea,
- C. niveiventris,
- Amazon,
- Type specimen

FullText(HTML)

References(50)

References

[1]	Boubli JP, Byrne H, da Silva MNF, Silva-Júnior J, Costa Araújo R, Bertuol F, et al. 2019. On a new species of titi monkey (Primates: Plecturocebus Byrne et al., 2016), from Alta Floresta, southern Amazon, Brazil. Molecular Phylogenetics and Evolution, 132: 117−137. doi: 10.1016/j.ympev.2018.11.012
[2]	Boubli JP, da Silva MNF, Rylands AB, Nash SD, Bertuol F, Nunes M, et al. 2018. How many pygmy marmoset (Cebuella Gray, 1870) species are there? A taxonomic re-appraisal based on new molecular evidence. Molecular Phylogenetics and Evolution, 120: 170−182. doi: 10.1016/j.ympev.2017.11.010
[3]	Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, et al. 2019. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15(4): e1006650. doi: 10.1371/journal.pcbi.1006650
[4]	Bouckaert RR, Drummond AJ. 2017. bModelTest: bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology, 17(1): 42. doi: 10.1186/s12862-017-0890-6
[5]	Burrell AS, Disotell TR, Bergey CM. 2015. The use of museum specimens with high-throughput DNA sequencers. Journal of Human Evolution, 79: 35−44. doi: 10.1016/j.jhevol.2014.10.015
[6]	Byrne H, Costa-Araújo R, Farias IP, Silva MNF, Messias M, Hrbek T, et al. 2021. Uncertainty regarding species delimitation, geographic distribution, and evolutionary history of titi monkey species (Plecturocebus, Pitheciidae) from southwestern Amazonia. International Journal of Primatology: in press
[7]	Chan KO, Hutter CR, Wood Jr PL, Grismer LL, Das I, Brown RM. 2020. Gene flow creates a mirage of cryptic species in a Southeast Asian spotted stream frog complex. Molecular Ecology, 29(20): 3970−3987. doi: 10.1111/mec.15603
[8]	da Cruz Lima E. 1945. Mammals of Amazonia. 1. General introduction and primates. Museu Paraense Emilio Goeldi de Historia Natural e Etnografia.
[9]	Dabney J, Knapp M, Glocke I, Gansauge MT, Weihmann A, Nickel B, et al. 2013. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proceedings of the National Academy of Sciences of the United States of America, 110(39): 15758−15763. doi: 10.1073/pnas.1314445110
[10]	Farias IP, Santos WG, Gordo M, Hrbek T. 2015. Effects of forest fragmentation on genetic diversity of the critically endangered primate, the pied tamarin (Saguinus bicolor): implications for conservation. Journal of Heredity, 106(Suppl1): 512−521.
[11]	Garbino GST, Casali DM, Nascimento FO, Serrano-Villavicencio JE. 2019. Taxonomy of the pygmy marmoset (Cebuella Gray, 1866): geographic variation, species delimitation, and nomenclatural notes. Mammalian Biology, 95: 135−142. doi: 10.1016/j.mambio.2018.09.003
[12]	Garcia-Erill G, Kjaer MM, Albrechtsen A, Siegismund HR, Heller R. 2021. Vicariance followed by secondary gene flow in a young gazelle species complex. Molecular Ecology, 30(2): 528−544. doi: 10.1111/mec.15738
[13]	Green RE, Krause J, Ptak SE, Briggs AW, Ronan MT, Simons JF, et al. 2006. Analysis of one million base pairs of Neanderthal DNA. Nature, 444(7117): 330−336. doi: 10.1038/nature05336
[14]	Groves CP. 2001. Primate Taxonomy. Washington DC: Smithsonian Institution Press.
[15]	Groves CP. 2005. Order primates. In: Wilson DE, Reeder DM. Mammal Species of the World: A Taxonomic and Geographic Reference. Baltimore, MD: Johns Hopkins University Press.
[16]	Haven Wiley R. 2010. Alfonso Olalla and his family: the ornithological exploration of Amazonian Peru. Bulletin of the American Museum of Natural History, 2010(343): 1−68.
[17]	Hershkovitz P. 1977. Living New World Monkeys (Platyrrhini) with An Introduction to Primates, Vol. 1. Chicago: University of Chicago Press.
[18]	Higuchi R, Bowman B, Freiberger M, Ryder OA, Wilson AC. 1984. DNA sequences from the quagga, an extinct member of the horse family. Nature, 312(5991): 282−284. doi: 10.1038/312282a0
[19]	Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4): 772−780. doi: 10.1093/molbev/mst010
[20]	Kay RF. 2015. Biogeography in deep time–what do phylogenetics, geology, and paleoclimate tell us about early platyrrhine evolution?. Molecular Phylogenetics and Evolution, 82: 358−374. doi: 10.1016/j.ympev.2013.12.002
[21]	Lamichhaney S, Han F, Webster MT, Grant BR, Grant PR, Andersson L. 2020. Female-biased gene flow between two species of Darwin’s finches. Nature Ecology & Evolution, 4(7): 979−986.
[22]	Lönnberg E. 1940. Notes on marmosets. Arkiv für Zoologi, 32A(10): 1−22.
[23]	Marsh LK. 2014. A taxonomic revision of the saki monkeys, Pithecia Desmarest, 1804. Neotropical Primates, 21(1): 1−165. doi: 10.1896/044.021.0101
[24]	Mittermeier RA, Wilson DE, Rylands AB. 2013. Handbook of the Mammals of the World: Primates. Barcelona: Lynx Edicions.
[25]	Moritz C. 1994. Defining ‘Evolutionarily Significant Units’ for conservation. Trends in Ecology & Evolution, 9(10): 373−375.
[26]	Naka LN, Bechtoldt CL, Henriques LMP, Brumfield RT. 2012. The role of physical barriers in the location of avian suture zones in the Guiana Shield, northern Amazonia. The American Naturalist, 179(4): E115−E132. doi: 10.1086/664627
[27]	Napier PH. 1976. Catalogue of Primates in the British Museum (Natural History). Part I: Families Callithricidae and Cebidae. London: British Museum (Natural History).
[28]	Noonan JP, Coop G, Kudaravalli S, Smith D, Krause J, Alessi J, et al. 2006. Sequencing and analysis of Neanderthal genomic DNA. Science, 314(5802): 1113−1118. doi: 10.1126/science.1131412
[29]	Orlando L, Metcalf JL, Alberdi MT, Telles-Antunes M, Bonjean D, Otte M, et al. 2009. Revising the recent evolutionary history of equids using ancient DNA. Proceedings of the National Academy of Sciences of the United States of America, 106(51): 21754−21759. doi: 10.1073/pnas.0903672106
[30]	Pääbo S. 1985. Molecular cloning of Ancient Egyptian mummy DNA. Nature, 314(6012): 644−645. doi: 10.1038/314644a0
[31]	Perri AR, Mitchell KJ, Mouton A, Álvarez-Carretero S, Hulme-Beaman A, Haile J, et al. 2021. Dire wolves were the last of an ancient New World canid lineage. Nature, 591(7848): 87−91. doi: 10.1038/s41586-020-03082-x
[32]	Porter LM, de la Torre S, Pérez-Peña P, Cortés-Ortiz L. 2021. Taxonomic diversity of Cebuella in the western Amazon: molecular, morphological and pelage diversity of museum and free-ranging specimens. American Journal of Physical Anthropology, 175(1): 251−267. doi: 10.1002/ajpa.24266
[33]	Prüfer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, et al. 2014. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature, 505(7481): 43−49. doi: 10.1038/nature12886
[34]	Rambaut A, Ho SYW, Drummond AJ, Shapiro B. 2009. Accommodating the effect of ancient DNA damage on inferences of demographic histories. Molecular Biology and Evolution, 26(2): 245−248. doi: 10.1093/molbev/msn256
[35]	Rohland N, Siedel H, Hofreiter M. 2004. Nondestructive DNA extraction method for mitochondrial DNA analyses of museum specimens. BioTechniques, 36(5): 814−821. doi: 10.2144/04365ST05
[36]	Roos C, Helgen KM, Miguez RP, Thant NML, Lwin N, Lin AK, et al. 2020. Mitogenomic phylogeny of the Asian colobine genus Trachypithecus with special focus on Trachypithecus phayrei (Blyth, 1847) and description of a new species. Zoological Research, 41(6): 656−669. doi: 10.24272/j.issn.2095-8137.2020.254
[37]	Rylands AB, Coimbra-Filho AF, Mittermeier RA. 2009. The systematics and distributions of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and callimico (Callimico) (Callitrichidae, Primates). In: Ford SM, Porter LM, Davis LC. The Smallest Anthropoids: The Marmoset/Callimico Radiation. Boston, MA: Springer, 25–61.
[38]	Sambrook J, Fritsch EF, Maniatis T. 1989. In vitro amplification of DNA by the polymerase chain reaction. In: Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 1431–1435.
[39]	Scheel DM, Slater GJ, Kolokotronis SO, Potter CW, Rotstein DS, Tsangaras K, et al. 2014. Biogeography and taxonomy of extinct and endangered monk seals illuminated by ancient DNA and skull morphology. ZooKeys, 409: 1−33. doi: 10.3897/zookeys.409.6244
[40]	Seiffert ER. 2006. Revised age estimates for the later Paleogene mammal faunas of Egypt and Oman. Proceedings of the National Academy of Sciences of the United States of America, 103(13): 5000−5005. doi: 10.1073/pnas.0600689103
[41]	Shepherd LD, Tennyson AJD, Lambert DM. 2013. Using ancient DNA to enhance museum collections: a case study of rare Kiwi (Apteryx spp. ) specimens. Journal of the Royal Society of New Zealand, 43(3): 119−127. doi: 10.1080/03036758.2012.732585
[42]	Soini P. 1988. The pygmy marmoset, Genus Cebuella. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, da Fonseca GAB. Ecology and Behavior of Neotropical Primates. Vol. 2. Washington, DC: World Wildlife Fund, 79–129.
[43]	Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9): 1312−1313. doi: 10.1093/bioinformatics/btu033
[44]	Swofford DL. 2002. PAUP*: Phylogenetic Analysis Using Parsimony, Version 4.0 b10. Sunderland, MA: Sinauer Associates.
[45]	van Roosmalen MGM, van Roosmalen T. 1997. An eastern extension of the geographical range of the pygmy marmoset. Cebuella pygmaea. Neotropical Primates, 5: 3−6.
[46]	Verry AJF, Scarsbrook L, Scofield RP, Tennyson AJD, Weston KA, Robertson BC, et al. 2019. Who, where, what, wren? Using ancient DNA to examine the veracity of museum specimen data: a case study of the New Zealand rock wren (Xenicus gilviventris). Frontiers in Ecology and Evolution, 7: 496. doi: 10.3389/fevo.2019.00496
[47]	von Spix JB. 1823. Simiarum et Vespertilionum Brasiliensium Species Novae. Munich: F. S. Hübschmann.
[48]	von Spix JB, von Martius KFP. 1824. Travels in Brazil, in the Years 1817-1820: Undertaken by Command of His Majesty the King of Bavaria. London: Longman, Hurst, Rees, Orme, Brown, and Green.
[49]	Weir JT, Faccio MS, Pulido-Santacruz P, Barrera-Guzmán AO, Aleixo A. 2015. Hybridization in headwater regions, and the role of rivers as drivers of speciation in Amazonian birds. Evolution, 69(7): 1823−1834. doi: 10.1111/evo.12696
[50]	Werle E, Schneider C, Renner M, Völker M, Fiehn W. 1994. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research, 22(20): 4354−4355. doi: 10.1093/nar/22.20.4354